Computational insights into the O2-evolving complex of photosystem II

Abstract

Mechanistic investigations of the water-splitting reaction of the oxygen-evolving complex (OEC) of photosystem II (PSII) are fundamentally informed by structural studies. Many physical techniques have provided important insights into the OEC structure and function, including X-ray diffraction (XRD) and extended X-ray absorption fine structure (EXAFS) spectroscopy as well as mass spectrometry (MS), electron paramagnetic resonance (EPR) spectroscopy and Fourier transform infrared spectroscopy applied in conjunction with mutagenesis studies. However, experimental studies have yet to yield consensus as to the exact configuration of the catalytic metal cluster and its ligation scheme. Computational modeling studies, including density functional (DFT) theory combined with quantum mechanics/molecular mechanics (QM/MM) hybrid methods for explicitly including the influence of the surrounding protein, have proposed chemically satisfactory models of the fully ligated OEC within PSII that are maximally consistent with experimental results. The inorganic core of these models is similar to the crystallographic model upon which they were based but comprises important modifications due to structural refinement, hydration and proteinaceous ligation which improve agreement with a wide range of experimental data. The computational models are useful for rationalizing spectroscopic and crystallographic results and for building a complete structure-based mechanism of water-splitting in PSII as described by the intermediate oxidation states of the OEC. This review summarizes these recent advances in QM/MM modeling of PSII within the context of recent experimental studies.

Functional models for the oxygen-evolving complex of photosystem II

“…D) OEC structure calculated using QM/MM methods and basic structural parameters from the 3.5 Å structure (figure was reproduced from ref. [32], with permission of the copyright holders). Schematic diagram of Kok's S-state cycle showing four oxidations necessary for water oxidation (figure was reproduced from ref.…”

“…In an effort to determine a more detailed structure of the OEC, quantum mechanical (QM) and molecular mechanics (MM) calculations were carried out that use the parameters of the 3.5 Å crystal structure and spectroscopic data [31][32][33]. Using a model including all residues within 15 Å of any of the OEC cluster atoms, a proposed structure for the OEC was calculated using (QM/MM) methods ( Figure 1D).…”

Comparison of Electrocatalysis and Bioelectrocatalysis of Hydrogen and Oxygen Redox Reactions

“…However, photosystem II does not appear to couple this with equal efficiently to the generation of a proton electrochemical gradient [113]; while CcO removes eight protons from the inside (bacterial cytoplasm, mitochondrial matrix) and adds four electrons to the outside, photosystem II removes four protons from the inside (stroma) for the reduction of the electron acceptor plastoquinone to plastoquinol, and adds the four protons from water to the outside (lumen) via proton exit channels [114].…”

“…The structures of the OEC in each redox state have therefore been optimized by combining DFT calculations with information derived from the large database of spectroscopic and enzymatic results. [110,111,113,114,[116][117][118]. Two types of DFT studies have been used to predict the geometric and electronic properties: Siegbahn and coworkers [113,116,117] used a cluster model with DFT employing the so-called B3LYP functional, and Batista and coworkers [114,118] used an embedded quantum mechanics/molecular mechanics (QM/MM) approach.…”

“…The net charges of the OEC plus ligands are given as superscripts. containing all Mn(IV) and an oxyl radical, according to Siegbahn and coworkers (a) [117], and Batista and coworkers (b) [114]. The geometries are simplified, and the protein-derived ligands are omitted to emphasize the cubic arrangement with a "dangling" manganese Mn4.…”